Integrative comparison of the genomic and transcriptomic landscape between prostate cancer patients of predominantly African or European genetic ancestry
Men of predominantly African Ancestry (AA) have higher prostate cancer (CaP) incidence and worse survival than men of predominantly European Ancestry (EA). While socioeconomic factors drive this disparity, genomic factors may also contribute to differences in the incidence and mortality rates. To co...
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| Published in | PLoS genetics Vol. 16; no. 2; p. e1008641 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
14.02.2020
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Men of predominantly African Ancestry (AA) have higher prostate cancer (CaP) incidence and worse survival than men of predominantly European Ancestry (EA). While socioeconomic factors drive this disparity, genomic factors may also contribute to differences in the incidence and mortality rates. To compare the prevalence of prostate tumor genomic alterations and transcriptomic profiles by patient genetic ancestry, we evaluated genomic profiles from The Cancer Genome Atlas (TCGA) CaP cohort (n = 498). Patient global and local genetic ancestry were estimated by computational algorithms using genotyping data; 414 (83.1%) were EA, 61 (12.2%) were AA, 11 (2.2%) were East Asian Ancestry (EAA), 10 (2.0%) were Native American (NA), and 2 (0.4%) were other ancestry. Genetic ancestry was highly concordant with self-identified race/ethnicity. Subsequent analyses were limited to 61 AA and 414 EA cases. Significant differences were observed by ancestry in the frequency of SPOP mutations (20.3% AA vs. 10.0% EA; p = 5.6×10-03), TMPRSS2-ERG fusions (29.3% AA vs. 39.6% EA; p = 4.4×10-02), and PTEN deletions/losses (11.5% AA vs. 30.2% EA; p = 3.5×10-03). Differentially expressed genes (DEGs) between AAs and EAs showed significant enrichment for prostate eQTL target genes (p = 8.09×10-48). Enrichment of highly expressed DEGs for immune-related pathways was observed in AAs, and for PTEN/PI3K signaling in EAs. Nearly one-third of DEGs (31.3%) were long non-coding RNAs (DE-lncRNAs). The proportion of DE-lncRNAs with higher expression in AAs greatly exceeded that with lower expression in AAs (p = 1.2×10-125). Both ChIP-seq and RNA-seq data suggested a stronger regulatory role for AR signaling pathways in DE-lncRNAs vs. non-DE-lncRNAs. CaP-related oncogenic lncRNAs, such as PVT1, PCAT1 and PCAT10/CTBP1-AS, were found to be more highly expressed in AAs. We report substantial heterogeneity in the prostate tumor genome and transcriptome between EA and AA. These differences may be biological contributors to racial disparities in CaP incidence and outcomes. |
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| AbstractList | Men of predominantly African Ancestry (AA) have higher prostate cancer (CaP) incidence and worse survival than men of predominantly European Ancestry (EA). While socioeconomic factors drive this disparity, genomic factors may also contribute to differences in the incidence and mortality rates. To compare the prevalence of prostate tumor genomic alterations and transcriptomic profiles by patient genetic ancestry, we evaluated genomic profiles from The Cancer Genome Atlas (TCGA) CaP cohort (n = 498). Patient global and local genetic ancestry were estimated by computational algorithms using genotyping data; 414 (83.1%) were EA, 61 (12.2%) were AA, 11 (2.2%) were East Asian Ancestry (EAA), 10 (2.0%) were Native American (NA), and 2 (0.4%) were other ancestry. Genetic ancestry was highly concordant with self-identified race/ethnicity. Subsequent analyses were limited to 61 AA and 414 EA cases. Significant differences were observed by ancestry in the frequency of SPOP mutations (20.3% AA vs. 10.0% EA; p = 5.6x10.sup.-03 ), TMPRSS2-ERG fusions (29.3% AA vs. 39.6% EA; p = 4.4x10.sup.-02 ), and PTEN deletions/losses (11.5% AA vs. 30.2% EA; p = 3.5x10.sup.-03). Differentially expressed genes (DEGs) between AAs and EAs showed significant enrichment for prostate eQTL target genes (p = 8.09x10.sup.-48). Enrichment of highly expressed DEGs for immune-related pathways was observed in AAs, and for PTEN/PI3K signaling in EAs. Nearly one-third of DEGs (31.3%) were long non-coding RNAs (DE-lncRNAs). The proportion of DE-lncRNAs with higher expression in AAs greatly exceeded that with lower expression in AAs (p = 1.2x10.sup.-125). Both ChIP-seq and RNA-seq data suggested a stronger regulatory role for AR signaling pathways in DE-lncRNAs vs. non-DE-lncRNAs. CaP-related oncogenic lncRNAs, such as PVT1, PCAT1 and PCAT10/CTBP1-AS, were found to be more highly expressed in AAs. We report substantial heterogeneity in the prostate tumor genome and transcriptome between EA and AA. These differences may be biological contributors to racial disparities in CaP incidence and outcomes. Men of predominantly African Ancestry (AA) have higher prostate cancer (CaP) incidence and worse survival than men of predominantly European Ancestry (EA). While socioeconomic factors drive this disparity, genomic factors may also contribute to differences in the incidence and mortality rates. To compare the prevalence of prostate tumor genomic alterations and transcriptomic profiles by patient genetic ancestry, we evaluated genomic profiles from The Cancer Genome Atlas (TCGA) CaP cohort (n = 498). Patient global and local genetic ancestry were estimated by computational algorithms using genotyping data; 414 (83.1%) were EA, 61 (12.2%) were AA, 11 (2.2%) were East Asian Ancestry (EAA), 10 (2.0%) were Native American (NA), and 2 (0.4%) were other ancestry. Genetic ancestry was highly concordant with self-identified race/ethnicity. Subsequent analyses were limited to 61 AA and 414 EA cases. Significant differences were observed by ancestry in the frequency of SPOP mutations (20.3% AA vs. 10.0% EA; p = 5.6×10-03), TMPRSS2-ERG fusions (29.3% AA vs. 39.6% EA; p = 4.4×10-02), and PTEN deletions/losses (11.5% AA vs. 30.2% EA; p = 3.5×10-03). Differentially expressed genes (DEGs) between AAs and EAs showed significant enrichment for prostate eQTL target genes (p = 8.09×10-48). Enrichment of highly expressed DEGs for immune-related pathways was observed in AAs, and for PTEN/PI3K signaling in EAs. Nearly one-third of DEGs (31.3%) were long non-coding RNAs (DE-lncRNAs). The proportion of DE-lncRNAs with higher expression in AAs greatly exceeded that with lower expression in AAs (p = 1.2×10-125). Both ChIP-seq and RNA-seq data suggested a stronger regulatory role for AR signaling pathways in DE-lncRNAs vs. non-DE-lncRNAs. CaP-related oncogenic lncRNAs, such as PVT1, PCAT1 and PCAT10/CTBP1-AS, were found to be more highly expressed in AAs. We report substantial heterogeneity in the prostate tumor genome and transcriptome between EA and AA. These differences may be biological contributors to racial disparities in CaP incidence and outcomes.Men of predominantly African Ancestry (AA) have higher prostate cancer (CaP) incidence and worse survival than men of predominantly European Ancestry (EA). While socioeconomic factors drive this disparity, genomic factors may also contribute to differences in the incidence and mortality rates. To compare the prevalence of prostate tumor genomic alterations and transcriptomic profiles by patient genetic ancestry, we evaluated genomic profiles from The Cancer Genome Atlas (TCGA) CaP cohort (n = 498). Patient global and local genetic ancestry were estimated by computational algorithms using genotyping data; 414 (83.1%) were EA, 61 (12.2%) were AA, 11 (2.2%) were East Asian Ancestry (EAA), 10 (2.0%) were Native American (NA), and 2 (0.4%) were other ancestry. Genetic ancestry was highly concordant with self-identified race/ethnicity. Subsequent analyses were limited to 61 AA and 414 EA cases. Significant differences were observed by ancestry in the frequency of SPOP mutations (20.3% AA vs. 10.0% EA; p = 5.6×10-03), TMPRSS2-ERG fusions (29.3% AA vs. 39.6% EA; p = 4.4×10-02), and PTEN deletions/losses (11.5% AA vs. 30.2% EA; p = 3.5×10-03). Differentially expressed genes (DEGs) between AAs and EAs showed significant enrichment for prostate eQTL target genes (p = 8.09×10-48). Enrichment of highly expressed DEGs for immune-related pathways was observed in AAs, and for PTEN/PI3K signaling in EAs. Nearly one-third of DEGs (31.3%) were long non-coding RNAs (DE-lncRNAs). The proportion of DE-lncRNAs with higher expression in AAs greatly exceeded that with lower expression in AAs (p = 1.2×10-125). Both ChIP-seq and RNA-seq data suggested a stronger regulatory role for AR signaling pathways in DE-lncRNAs vs. non-DE-lncRNAs. CaP-related oncogenic lncRNAs, such as PVT1, PCAT1 and PCAT10/CTBP1-AS, were found to be more highly expressed in AAs. We report substantial heterogeneity in the prostate tumor genome and transcriptome between EA and AA. These differences may be biological contributors to racial disparities in CaP incidence and outcomes. Men of predominantly African Ancestry (AA) have higher prostate cancer (CaP) incidence and worse survival than men of predominantly European Ancestry (EA). While socioeconomic factors drive this disparity, genomic factors may also contribute to differences in the incidence and mortality rates. To compare the prevalence of prostate tumor genomic alterations and transcriptomic profiles by patient genetic ancestry, we evaluated genomic profiles from The Cancer Genome Atlas (TCGA) CaP cohort (n = 498). Patient global and local genetic ancestry were estimated by computational algorithms using genotyping data; 414 (83.1%) were EA, 61 (12.2%) were AA, 11 (2.2%) were East Asian Ancestry (EAA), 10 (2.0%) were Native American (NA), and 2 (0.4%) were other ancestry. Genetic ancestry was highly concordant with self-identified race/ethnicity. Subsequent analyses were limited to 61 AA and 414 EA cases. Significant differences were observed by ancestry in the frequency of SPOP mutations (20.3% AA vs. 10.0% EA; p = 5.6×10-03), TMPRSS2-ERG fusions (29.3% AA vs. 39.6% EA; p = 4.4×10-02), and PTEN deletions/losses (11.5% AA vs. 30.2% EA; p = 3.5×10-03). Differentially expressed genes (DEGs) between AAs and EAs showed significant enrichment for prostate eQTL target genes (p = 8.09×10-48). Enrichment of highly expressed DEGs for immune-related pathways was observed in AAs, and for PTEN/PI3K signaling in EAs. Nearly one-third of DEGs (31.3%) were long non-coding RNAs (DE-lncRNAs). The proportion of DE-lncRNAs with higher expression in AAs greatly exceeded that with lower expression in AAs (p = 1.2×10-125). Both ChIP-seq and RNA-seq data suggested a stronger regulatory role for AR signaling pathways in DE-lncRNAs vs. non-DE-lncRNAs. CaP-related oncogenic lncRNAs, such as PVT1, PCAT1 and PCAT10/CTBP1-AS, were found to be more highly expressed in AAs. We report substantial heterogeneity in the prostate tumor genome and transcriptome between EA and AA. These differences may be biological contributors to racial disparities in CaP incidence and outcomes. Men of predominantly African Ancestry (AA) have higher prostate cancer (CaP) incidence and worse survival than men of predominantly European Ancestry (EA). While socioeconomic factors drive this disparity, genomic factors may also contribute to differences in the incidence and mortality rates. To compare the prevalence of prostate tumor genomic alterations and transcriptomic profiles by patient genetic ancestry, we evaluated genomic profiles from The Cancer Genome Atlas (TCGA) CaP cohort (n = 498). Patient global and local genetic ancestry were estimated by computational algorithms using genotyping data; 414 (83.1%) were EA, 61 (12.2%) were AA, 11 (2.2%) were East Asian Ancestry (EAA), 10 (2.0%) were Native American (NA), and 2 (0.4%) were other ancestry. Genetic ancestry was highly concordant with self-identified race/ethnicity. Subsequent analyses were limited to 61 AA and 414 EA cases. Significant differences were observed by ancestry in the frequency of SPOP mutations (20.3% AA vs. 10.0% EA; p = 5.6×10 −03 ), TMPRSS2-ERG fusions (29.3% AA vs. 39.6% EA; p = 4.4×10 −02 ), and PTEN deletions/losses (11.5% AA vs. 30.2% EA; p = 3.5×10 −03 ). Differentially expressed genes (DEGs) between AAs and EAs showed significant enrichment for prostate eQTL target genes (p = 8.09×10 −48 ). Enrichment of highly expressed DEGs for immune-related pathways was observed in AAs, and for PTEN/PI3K signaling in EAs. Nearly one-third of DEGs (31.3%) were long non-coding RNAs (DE-lncRNAs). The proportion of DE-lncRNAs with higher expression in AAs greatly exceeded that with lower expression in AAs (p = 1.2×10 −125 ). Both ChIP-seq and RNA-seq data suggested a stronger regulatory role for AR signaling pathways in DE-lncRNAs vs. non-DE-lncRNAs. CaP-related oncogenic lncRNAs, such as PVT1 , PCAT1 and PCAT10/CTBP1-AS , were found to be more highly expressed in AAs. We report substantial heterogeneity in the prostate tumor genome and transcriptome between EA and AA. These differences may be biological contributors to racial disparities in CaP incidence and outcomes. Disparities in cancer defined by self-identified race or ethnicity have been a long-standing and persistent challenge. It is well documented that certain racial and ethnic populations in the US experience higher incidence of specific cancer types, higher incidence of aggressive cancers, and higher mortality. The Cancer Genome Atlas (TCGA) data resource contains multi-omic profiles and clinical annotations of large-scale samples, and therefore serves as an excellent resource for the evaluation of the relationship between genetic ancestry and genomic alterations in cancers. In this study, we performed a cancer type specific analysis of the influence of genetic ancestry on genomic alterations in prostate cancers–a malignancy for which there are some of the largest cancer disparities by race and ethnicity in the US. We found that there is substantial heterogeneity in the genomic alterations and transcriptomic dysregulation occurring in men of African (AA) and European (EA) ancestry in the TCGA prostate cancer cohort. SPOP mutations, TMPRSS2-ERG fusions, PTEN deletions/losses, immune signaling, and expression of non-coding RNAs were identified as potential contributors to prostate cancer racial disparities. Our comprehensive characterization of genetic ancestry and genomic/transcriptomic alterations would provide new insight into the biology of prostate cancer racial disparities in the AA population. Men of predominantly African Ancestry (AA) have higher prostate cancer (CaP) incidence and worse survival than men of predominantly European Ancestry (EA). While socioeconomic factors drive this disparity, genomic factors may also contribute to differences in the incidence and mortality rates. To compare the prevalence of prostate tumor genomic alterations and transcriptomic profiles by patient genetic ancestry, we evaluated genomic profiles from The Cancer Genome Atlas (TCGA) CaP cohort (n = 498). Patient global and local genetic ancestry were estimated by computational algorithms using genotyping data; 414 (83.1%) were EA, 61 (12.2%) were AA, 11 (2.2%) were East Asian Ancestry (EAA), 10 (2.0%) were Native American (NA), and 2 (0.4%) were other ancestry. Genetic ancestry was highly concordant with self-identified race/ethnicity. Subsequent analyses were limited to 61 AA and 414 EA cases. Significant differences were observed by ancestry in the frequency of SPOP mutations (20.3% AA vs. 10.0% EA; p = 5.6×10−03), TMPRSS2-ERG fusions (29.3% AA vs. 39.6% EA; p = 4.4×10−02), and PTEN deletions/losses (11.5% AA vs. 30.2% EA; p = 3.5×10−03). Differentially expressed genes (DEGs) between AAs and EAs showed significant enrichment for prostate eQTL target genes (p = 8.09×10−48). Enrichment of highly expressed DEGs for immune-related pathways was observed in AAs, and for PTEN/PI3K signaling in EAs. Nearly one-third of DEGs (31.3%) were long non-coding RNAs (DE-lncRNAs). The proportion of DE-lncRNAs with higher expression in AAs greatly exceeded that with lower expression in AAs (p = 1.2×10−125). Both ChIP-seq and RNA-seq data suggested a stronger regulatory role for AR signaling pathways in DE-lncRNAs vs. non-DE-lncRNAs. CaP-related oncogenic lncRNAs, such as PVT1, PCAT1 and PCAT10/CTBP1-AS, were found to be more highly expressed in AAs. We report substantial heterogeneity in the prostate tumor genome and transcriptome between EA and AA. These differences may be biological contributors to racial disparities in CaP incidence and outcomes. |
| Audience | Academic |
| Author | Yuan, Jiao Rebbeck, Timothy R. Zhang, Youyou Hu, Xiaowen Fan, Yi Kensler, Kevin H. Tanyi, Janos L. Zhang, Lin Hu, Zhongyi Zhang, Rugang Jiang, Junjie Xu, Mu Pan, Yutian Zhang, Tianli Long, Meixiao Montone, Kathleen T. |
| AuthorAffiliation | 7 Department of Radiation Oncology, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America 3 Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts, United States of America 8 Wistar Institute, Philadelphia, Pennsylvania, United States of America St Jude Children's Research Hospital, UNITED STATES 4 Department of Epidemiology, Harvard TH Chan School of Public Health, Boston, Massachusetts, United States of America 1 Center for Research on Reproduction & Women’s Health, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America 2 Department of Obstetrics and Gynecology, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America 5 Department of Internal Medicine, Division of Hematology, Ohio State University, Columbus, Ohio, United States of America 6 Department of Pathology and Laboratory Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America |
| AuthorAffiliation_xml | – name: 1 Center for Research on Reproduction & Women’s Health, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America – name: St Jude Children's Research Hospital, UNITED STATES – name: 7 Department of Radiation Oncology, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America – name: 2 Department of Obstetrics and Gynecology, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America – name: 4 Department of Epidemiology, Harvard TH Chan School of Public Health, Boston, Massachusetts, United States of America – name: 3 Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts, United States of America – name: 8 Wistar Institute, Philadelphia, Pennsylvania, United States of America – name: 5 Department of Internal Medicine, Division of Hematology, Ohio State University, Columbus, Ohio, United States of America – name: 6 Department of Pathology and Laboratory Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America |
| Author_xml | – sequence: 1 givenname: Jiao orcidid: 0000-0003-2597-2319 surname: Yuan fullname: Yuan, Jiao – sequence: 2 givenname: Kevin H. orcidid: 0000-0001-7515-7270 surname: Kensler fullname: Kensler, Kevin H. – sequence: 3 givenname: Zhongyi surname: Hu fullname: Hu, Zhongyi – sequence: 4 givenname: Youyou surname: Zhang fullname: Zhang, Youyou – sequence: 5 givenname: Tianli surname: Zhang fullname: Zhang, Tianli – sequence: 6 givenname: Junjie surname: Jiang fullname: Jiang, Junjie – sequence: 7 givenname: Mu surname: Xu fullname: Xu, Mu – sequence: 8 givenname: Yutian surname: Pan fullname: Pan, Yutian – sequence: 9 givenname: Meixiao surname: Long fullname: Long, Meixiao – sequence: 10 givenname: Kathleen T. orcidid: 0000-0002-5794-3371 surname: Montone fullname: Montone, Kathleen T. – sequence: 11 givenname: Janos L. surname: Tanyi fullname: Tanyi, Janos L. – sequence: 12 givenname: Yi surname: Fan fullname: Fan, Yi – sequence: 13 givenname: Rugang orcidid: 0000-0002-7255-2360 surname: Zhang fullname: Zhang, Rugang – sequence: 14 givenname: Xiaowen surname: Hu fullname: Hu, Xiaowen – sequence: 15 givenname: Timothy R. orcidid: 0000-0002-4799-1900 surname: Rebbeck fullname: Rebbeck, Timothy R. – sequence: 16 givenname: Lin orcidid: 0000-0003-1998-0611 surname: Zhang fullname: Zhang, Lin |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32059012$$D View this record in MEDLINE/PubMed |
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| Copyright | COPYRIGHT 2020 Public Library of Science 2020 Yuan et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2020 Yuan et al 2020 Yuan et al |
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| Notes | new_version ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 I have read the journal's policy and the authors of this manuscript have the following competing interests: Drs. Lin Zhang and Xiaowen Hu received research grant from Bristol-Myers Squibb/Celgene. The other authors declare no potential conflicts of interest. |
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| SubjectTerms | 1-Phosphatidylinositol 3-kinase Algorithms Biology and Life Sciences Biomarkers, Tumor - genetics Biomarkers, Tumor - metabolism Black or African American - genetics Cancer genetics Care and treatment Chromatin Immunoprecipitation Sequencing Cohort Studies Comparative analysis Computer applications Epidemiology Ethnicity Gene expression Gene Expression Regulation, Neoplastic Genes Genetic aspects Genome, Human - genetics Genomes Genomics Genotyping Gynecology Health aspects Health Status Disparities Hispanic Americans Humans Incidence Male Medicine and Health Sciences Middle Aged Minority & ethnic groups Mortality Mutation Native Americans Non-coding RNA Nuclear Proteins - genetics Obstetrics Oncogene Proteins, Fusion - genetics Oncology Patients Prevalence studies (Epidemiology) Prostate cancer Prostatic Neoplasms - epidemiology Prostatic Neoplasms - genetics PTEN Phosphohydrolase - genetics PTEN protein Public health Race Racial differences Receptors, Androgen - genetics Repressor Proteins - genetics Ribonucleic acid RNA RNA, Long Noncoding - metabolism RNA-Seq Signal transduction Socioeconomic factors Transcriptome - genetics Transcriptomics Tumors White People - genetics |
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| Title | Integrative comparison of the genomic and transcriptomic landscape between prostate cancer patients of predominantly African or European genetic ancestry |
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